Experimental Brain Research

, Volume 172, Issue 3, pp 343–350 | Cite as

Asymmetric short-term adaptation of the vertical vestibulo-ocular reflex in humans

  • Sarah Marti
  • Christopher J. Bockisch
  • Dominik Straumann
Research Article


Anatomical and electrophysiological studies have demonstrated up–down asymmetries in vertical ocular motor pathways. We investigated whether these asymmetries extend to the capacity for short-term adaptation of the vertical vestibulo-ocular reflex (VVOR) in humans. Specifically, we asked whether smooth pursuit signals are sufficient to asymmetrically adapt the VVOR. Healthy human subjects (N=8), positioned 90° left-ear-down and fixating with their eyes upon a small laser dot (diameter: 0.1°) projected on a sphere (distance: 1.4 m) were trained toward low VVOR gain for 30 min with symmetric and asymmetric visual VVOR cancellation paradigms, while being oscillated (0.2 Hz, ±20°) on a motorized turntable about the interaural earth-vertical axis. During asymmetric VVOR cancellation, the target was head-fixed in either the pitch-up or pitch-down half-cycles of oscillation (=trained direction) and space-fixed during the other half-cycles (=untrained direction). During symmetric VVOR cancellation, the target was head-fixed throughout the oscillations. Before and after adaptation, the pitch-up and pitch-down VOR gains were assessed during turntable oscillation in complete darkness. Before adaptation, average gains of pitch-up (0.75±0.15 SD) and pitch-down (0.79±0.19 SD) VOR were not significantly different (paired t test: P>0.05). On an average, relative gain reductions induced by selective pitch-up (pitch-up VOR: 32%; pitch-down VOR: 21%) and pitch-down (pitch-up VOR: 18%; pitch-down VOR: 30%) VOR cancellation were significantly (P<0.05) larger in the trained than in the untrained direction. Symmetric visual VVOR cancellation led to a significantly (P<0.01) larger relative gain reduction of the pitch-down (41%) than the pitch-up (33%) VOR. None of the paradigms led to significant changes of phase or offset. We conclude that, in human subjects, the smooth pursuit system is capable to asymmetrically decrease the gain of the VVOR equally well in both the upward and downward direction. The unexpected asymmetric decrease of the VVOR gain after symmetric visual cancellation may be related to the directional preferences of vertical gaze–velocity sensitive Purkinje cells in the flocculus for the downward direction.


Smooth Pursuit Gain Reduction Adaptation Paradigm Asymmetric Adaptation Internuclear Ophthalmoplegia 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



The authors thank Dr. T. Haslwanter for his valuable comments; T. Schmückle, E. Schafflützel, and A. Züger for technical assistance.


  1. Baloh RW, Demer J (1991) Gravity and the vertical vestibulo-ocular reflex. Exp Brain Res 83:427–433PubMedCrossRefGoogle Scholar
  2. Baloh RW, Honrubia V, Yee RD, Jacobson K (1986) Vertical visual–vestibular interaction in normal human subjects. Exp Brain Res 64:400–406PubMedCrossRefGoogle Scholar
  3. Bergamin O, Zee DS, Roberts DC, Landau K, Lasker AG, Straumann D (2001) Three-dimensional Hess screen test with binocular dual search coils in a three-field magnetic system. Invest Ophthalmol Vis Sci 42:660–667PubMedGoogle Scholar
  4. Bisdorff AR, Sancovic S, Debatisse D, Bentley C, Gresty MA, Bronstein AM (2000) Positional nystagmus in the dark in normal subjects. Neuroophthalmology 24:283–290Google Scholar
  5. Blazquez P, Partsalis A, Gerrits NM, Highstein SM (2000) Input of anterior and posterior semicircular canal interneurons encoding head-velocity to the dorsal Y group of the vestibular nuclei. J Neurophysiol 83:2891–2904PubMedGoogle Scholar
  6. Chubb MC, Fuchs AF (1982) Contribution of y group of vestibular nuclei and dentate nucleus of cerebellum to generation of vertical smooth eye movements. J Neurophysiol 48:75–99PubMedGoogle Scholar
  7. Cremer PD, Migliaccio AA, Halmagyi GM, Curthoys IS (1999) Vestibulo-ocular reflex pathways in internuclear ophthalmoplegia. Ann Neurol 45:529–533PubMedCrossRefGoogle Scholar
  8. Darlot C, Lopez-Barneo J, Tracey D (1981) Asymmetries of vertical vestibular nystagmus in the cat. Exp Brain Res 41:420–426PubMedCrossRefGoogle Scholar
  9. Demer JL (1992) Mechanisms of human vertical visual–vestibular interaction. J Neurophysiol 68:2128–2146PubMedGoogle Scholar
  10. Demer JL, Porter FI, Goldberg J, Jenkins HA, Schmidt K (1989) Adaptation to telescopic spectacles: vestibulo-ocular reflex plasticity. Invest Ophthalmol Vis Sci 30:159–170PubMedGoogle Scholar
  11. Fukushima K, Fukushima J, Kaneko CR, Fuchs AF (1999) Vertical Purkinje cells of the monkey floccular lobe: simple-spike activity during pursuit and passive whole body rotation. J Neurophysiol 82:787–803PubMedGoogle Scholar
  12. Halmagyi GM, Rudge P, Gresty MA, Sanders MD (1983) Downbeating nystagmus. A review of 62 cases. Arch Neurol 40:777–784PubMedGoogle Scholar
  13. Hepp K (1990) On Listing’s law. Commun Math Phys 132:285–292CrossRefGoogle Scholar
  14. Hirata Y, Highstein SM (2001) Acute adaptation of the vestibuloocular reflex: signal processing by floccular and ventral parafloccular Purkinje cells. J Neurophysiol 85:2267–2288PubMedGoogle Scholar
  15. Hirata Y, Highstein SM (2002) Plasticity of the vertical VOR: a system identification approach to localizing the adaptive sites. Ann N Y Acad Sci 978:480–495PubMedCrossRefGoogle Scholar
  16. Hirata Y, Lockard JM, Highstein SM (2002) Capacity of vertical VOR adaptation in squirrel monkey. J Neurophysiol 88:3194–3207PubMedCrossRefGoogle Scholar
  17. Huebner WP, Leigh RJ, Seidman SH, Thomas CW, Billian C, DiScenna AO, Dell’Osso LF (1992) Experimental tests of a superposition hypothesis to explain the relationship between the vestibuloocular reflex and smooth pursuit during horizontal combined eye-head tracking in humans. J Neurophysiol 68:1775–1792PubMedGoogle Scholar
  18. Ito M (1972) Neural design of the cerebellar motor control system. Brain Res 40:81–84PubMedCrossRefGoogle Scholar
  19. Ito M (1982) Cerebellar control of the vestibulo-ocular reflex—around the flocculus hypothesis. Annu Rev Neurosci 5:275–296PubMedCrossRefGoogle Scholar
  20. Ito M, Nisimaru N, Yamamoto M (1977) Specific patterns of neuronal connexions involved in the control of the rabbit’s vestibulo-ocular reflexes by the cerebellar flocculus. J Physiol (London) 265:833–854Google Scholar
  21. Kim JS, Sharpe JA (2001) The vertical vestibulo-ocular reflex, and its interaction with vision during active head motion: effects of aging. J Vestib Res 11:3–12PubMedGoogle Scholar
  22. Kramer PD, Shelhamer M, Peng GC, Zee DS (1998) Context-specific short-term adaptation of the phase of the vestibulo-ocular reflex. Exp Brain Res 120:184–192PubMedCrossRefGoogle Scholar
  23. Lanman J, Bizzi E, Allum J (1978) The coordination of eye and head movement during smooth pursuit. Brain Res 153:39–53PubMedCrossRefGoogle Scholar
  24. Leigh RJ, Zee DS (1999) The neurology of eye movements, 3rd edn. Oxford University Press, OxfordGoogle Scholar
  25. Lisberger SG (1990) Visual tracking in monkeys: evidence for short-latency suppression of the vestibuloocular reflex. J Neurophysiol 63:676–688PubMedGoogle Scholar
  26. Lisberger SG, Pavelko TA, Bronte-Stewart HM, Stone LS (1994a) Neural basis for motor learning in the vestibuloocular reflex of primates. II. Changes in the responses of horizontal gaze velocity Purkinje cells in the cerebellar flocculus and ventral paraflocculus. J Neurophysiol 72:954–973Google Scholar
  27. Lisberger SG, Pavelko TA, Broussard DM (1994b) Neural basis for motor learning in the vestibuloocular reflex of primates. I. Changes in the responses of brain stem neurons. J Neurophysiol 72:928–953Google Scholar
  28. Marti S, Palla A, Straumann D (2002) Gravity dependence of ocular drift in patients with cerebellar downbeat nystagmus. Ann Neurol 52:712–721PubMedCrossRefGoogle Scholar
  29. Matsuo V, Cohen B (1984) Vertical optokinetic nystagmus and vestibular nystagmus in the monkey: up–down asymmetry and effects of gravity. Exp Brain Res 53:197–216PubMedCrossRefGoogle Scholar
  30. Melvill JG, Guitton D, Berthoz A (1988) Changing patterns of eye–head coordination during 6 h of optically reversed vision. Exp Brain Res 69:531–544CrossRefGoogle Scholar
  31. Miles FA, Fuller JH, Braitman DJ, Dow BM (1980) Long-term adaptive changes in primate vestibuloocular reflex. III. Electrophysiological observations in flocculus of normal monkeys. J Neurophysiol 43:1437–1476PubMedGoogle Scholar
  32. Miles FA, Lisberger SG (1981a) The “error” signals subserving adaptive gain control in the primate vestibulo-ocular reflex. Ann N Y Acad Sci 374:513–525PubMedCrossRefGoogle Scholar
  33. Miles FA, Lisberger SG (1981b) Plasticity in the vestibulo-ocular reflex: a new hypothesis. Annu Rev Neurosci 4:273–299PubMedCrossRefGoogle Scholar
  34. Paige GD, Sargent EW (1991) Visually-induced adaptive plasticity in the human vestibulo-ocular reflex. Exp Brain Res 84:25–34PubMedCrossRefGoogle Scholar
  35. Partsalis AM, Zhang Y, Highstein SM (1995a) Dorsal Y group in the squirrel monkey. I. Neuronal responses during rapid and long-term modifications of the vertical VOR. J Neurophysiol 73:615–631PubMedGoogle Scholar
  36. Partsalis AM, Zhang Y, Highstein SM (1995b) Dorsal Y group in the squirrel monkey. II. Contribution of the cerebellar flocculus to neuronal responses in normal and adapted animals. J Neurophysiol 73:632–650PubMedGoogle Scholar
  37. Peng GC, Baker JF, Peterson BW (1994) Dynamics of directional plasticity in the human vertical vestibulo-ocular reflex. J Vestib Res 4:453–460PubMedGoogle Scholar
  38. Schmid-Priscoveanu A, Straumann D, Kori AA (2000) Torsional vestibulo-ocular reflex during whole-body oscillation in the upright and the supine position. I. Responses in healthy human subjects. Exp Brain Res 134:212–219PubMedCrossRefGoogle Scholar
  39. Shelhamer M, Tiliket C, Roberts D, Kramer PD, Zee DS (1994) Short-term vestibulo-ocular reflex adaptation in humans. II. Error signals. Exp Brain Res 100:328–336PubMedCrossRefGoogle Scholar
  40. Snyder LH, King WM (1988) Vertical vestibuloocular reflex in cat: asymmetry and adaptation. J Neurophysiol 59:279–298PubMedGoogle Scholar
  41. Stone LS, Lisberger SG (1990) Visual responses of Purkinje cells in the cerebellar flocculus during smooth-pursuit eye movements in monkeys. I. Simple spikes. J Neurophysiol 63:1241–1261PubMedGoogle Scholar
  42. Tiliket C, Shelhamer M, Roberts D, Zee DS (1994) Short-term vestibulo-ocular reflex adaptation in humans. I. Effect on the ocular motor velocity-to-position neural integrator. Exp Brain Res 100:316–327PubMedCrossRefGoogle Scholar
  43. Trillenberg P, Shelhamer M, Roberts DC, Zee DS (2003) Cross-axis adaptation of torsional components in the yaw-axis vestibulo-ocular reflex. Exp Brain Res 148:158–165PubMedGoogle Scholar
  44. Viirre ES, Demer JL (1996) The human vertical vestibulo-ocular reflex during combined linear and angular acceleration with near-target fixation. Exp Brain Res 112:313–324PubMedCrossRefGoogle Scholar
  45. Watanabe E (1984) Neuronal events correlated with long-term adaptation of the horizontal vestibulo-ocular reflex in the primate flocculus. Brain Res 297:169–174PubMedCrossRefGoogle Scholar
  46. Watanabe E (1985) Role of the primate flocculus in adaptation of the vestibulo-ocular reflex. Neurosci Res 3:20–38PubMedCrossRefGoogle Scholar
  47. Zee DS, Friendlich AR, Robinson DA (1974) The mechanism of downbeat nystagmus. Arch Neurol 30:227–237PubMedGoogle Scholar
  48. Zee DS, Yee RD, Cogan DG, Robinson DA, Engel WK (1976) Ocular motor abnormalities in hereditary cerebellar ataxia. Brain 99:207–234PubMedCrossRefGoogle Scholar
  49. Zee DS, Yamazaki A, Butler PH, Gucer G (1981) Effects of ablation of flocculus and paraflocculus of eye movements in primate. J Neurophysiol 46:878–899PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Sarah Marti
    • 1
  • Christopher J. Bockisch
    • 1
    • 2
  • Dominik Straumann
    • 1
  1. 1.Neurology DepartmentZurich University HospitalZurichSwitzerland
  2. 2.Departments of Ophthalmology and OtolaryngologyZurich University HospitalZurichSwitzerland

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